Published online 24 January 2006
Published in Crop Sci 46:404-412 (2006)
© 2006 Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
FORAGE & GRAZINGLANDS
Temperature Influences on Endophyte Growth in Tall Fescue
H.-J. Jua,
N. S. Hilla,*,
T. Abbottb and
K. T. Ingramc
a Dep. of Crop and Soil Science, Univ. of Georgia, Athens, GA 30602
b Pennington Seed Co., Lebanon, OR
c Dep. of Agricultural and Biological Engineering, Univ. of Florida, Gainesville, FL 32611
* Corresponding author (nhill{at}uga.edu)
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ABSTRACT
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Tall fescue (Festuca arundinacea Schreb.) is the predominant perennial cool-season grass grown in the USA. Typically, tall fescue is infected with the endophyte, Neotyphodium coenophialum Morgan-Jones & Gams, which produces alkaloids that are toxic to grazing animals. Nontoxic endophyte-infected cultivars of tall fescue have been developed, but to maximize their utility for profitable livestock production a better understanding of conditions affecting seed and tiller transmission is needed to maintain endophytes in seed. Our understanding of mechanisms of endophyte transmission in planta is limited. Seasonal variations of endophyte in established tall fescue pastures in Watkinsville, GA, and seed fields near Salem, OR, were examined. Growth chamber experiments were conducted to examine temperature effects on plant and endophyte growth and to determine the cardinal minimum temperatures for each. Endophyte frequency varied over months in both Georgia and Oregon. Frequency averaged 93.4% when sampled April through December, but was 80.5% when sampled January through March in Georgia. Frequency averaged 64.5% when sampled February through April, but was 88.6% during other months in Oregon. Cardinal minimum temperature for plant growth was 5.2°C (± 0.5), but for endophyte was 10.3°C (± 0.7). Temperature appears to be a major variable affecting fluctuation of endophyte frequency in plant tissue.
Abbreviations: LSD, least significant difference.
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INTRODUCTION
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TALL FESCUE is the predominant cool-season perennial grass grown in the USA. It is frequently infected with the endophytic fungus, N. coenophialum (Bacon and Siegel, 1988). The endophyte receives nutrition and structural refuge from the host, while the host receives benefits such as enhanced competitiveness (Hill et al., 1991, 1998; Malinowski et al., 1999) from more efficient water utilization through increasing leaf rolling (Arachevaleta et al., 1989), and decreasing stomatal conductance (Elmi and West, 1995; Elbersen and West, 1996). Thus, the two organisms are in a mutualistic relationship.
Animals grazing endophyte-infected tall fescue consume endophyte-derived ergot alkaloids resulting in reduced animal performance (Hoveland, 1993; Read and Camp, 1986). Recently, nontoxic endophytes have been inserted into tall fescue to capitalize on the agronomic benefit of the endophyte, but eliminate the toxicity to grazing livestock (Bouton, 2000; Bouton et al., 2002; Fletcher, 1999). Endophytes have been historically viewed as negative components of the pasture ecosystem (Ball et al., 1996), but emerging use of nontoxic endophytes has resulted in a positive connotation for cultivar development (Bouton et al., 2002; Fletcher, 1999). Therefore, it is vital to understand endophyte growth and transmission in cool-season grasses to maximize the probability of maintaining nontoxic endophytes as well as accurately characterize pastures that are candidates for reseeding.
The endophyte life cycle is relatively simple because it has no sexual stage, produces no spores, and disseminates only in the seed though the female parent (Siegel et al., 1984). Di Menna and Waller (1986) found seasonal variation in mycelium concentration of N. lolii Latch, Christensen & Samuels in leaf sheaths of perennial ryegrass (Lolium perenne L.). Bacon and Siegel (1988) reported a decrease in endophyte level in seed after a hot and dry summer and cold winter. While these studies suggest environmental parameters affect endophyte growth and transmission, direct evidence is lacking. Therefore, the objectives of this study were to examine (i) seasonal variation of endophyte infection within tall fescue, and (ii) temperature effects on endophyte growth in planta.
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MATERIALS AND METHODS
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Experiment 1. Seasonal Variation of Endophyte in Tall Fescue
Two hundred tillers were randomly sampled from two established pastures of ‘Jesup’ MaxQ while walking across each. Sampling began on 1 July 2000 and continued on the first of each month until 1 June 2002. Both pastures were replications within a larger grazing study located in Watkinsville, GA. In a separate study, 200 tillers were sampled from two seed production fields of Jesup MaxQ growing in the central Willamette Valley of Oregon on the first of each month from October 1999 to May 2000 and from October 2000 to May 2001. Sampling was not performed from June through September in Oregon because of interference with seed harvest or lack of vegetative growth.
A 2- to 3-mm cross section of each tiller base was tested for endophyte frequency within each sampling date and each location using a commercial immunoblot test kit (Agrinostics Ltd. Co., Watkinsville, GA). The Georgia samples were analyzed for endophyte concentration at the pseudostem base (bottom) and 3 cm above the pseudostem base (middle) using ELISA (Hiatt et al., 1997). Weather data were obtained from a weather station located next to the pastures in Georgia and from a weather station located in Salem, OR, approximately 18 km from the seed production field.
The data on frequency of infection from both studies were analyzed by the PROC MIXED subroutine of the analysis of variance procedure of SAS (SAS Institute, Cary, NC). The analysis of variance model was a complete factorial of year and month as treatment variables in a randomized complete block design. Fields within each location were used as replicates. Months were considered a fixed effect, whereas years (environments) were considered random effects. Data for endophyte concentration (Georgia only) were analyzed using the PROC MIXED subroutine of the analysis of variance procedure in SAS. The analysis of variance model was a complete factorial of year, month, and location within pseudostem treatment variables. Sample location within the pseudostem and months were considered fixed effects, whereas years (environments) were considered random effects. The two fields sampled served as replicates. All treatment means were separated using a Fisher's protected least significant difference (LSD) at 
= 0.05. There were no year effects or interactions within years for either the Georgia or Oregon sites, so data from the 2 yr were pooled and reanalyzed for replicate and month effects. A paired Student's t test was used to determine the effect of sampling location in the plant on endophyte detection for the Georgia samples. Endophyte frequency for samples collected in Georgia and Oregon, and endophyte concentration data for samples collected in Georgia were correlated with mean monthly temperature and precipitation using the PROC CORR subroutine of SAS.
Experiment 2. Temperature Effects on Endophyte Growth
Growth Response of Endophyte and Tall Fescue under Different Temperature Regimes
Seeds of Jesup MaxQ were placed in water and incubated at 4°C for 7 d to break dormancy. Seventy-two seeds were planted into each of 36 flats containing a commercial germinating mix (Fafard) (Conrad Fafard, Inc., Agawam, MA), and placed into a greenhouse until germinated. Thirty-six flats of 7-d-old seedlings were randomly assigned to 12 treatments consisting of a factorial combination of four temperature regimes and three harvest dates. The three harvest dates occurred 0, 3, and 6 wk after germination. The four temperature regimes were (i) 12/6°C day/night temperature for 3 wk followed by 25/19°C day/night temperature for 3 wk; (ii) 25/19°C day/night temperature for 3 wk followed by 12/6°C day/night temperature for 3 wk; (iii) 12/6°C day/night temperature for 6 wk; and (iv) 25/19°C day/night temperature for 6 wk.
Germination date was recorded when 50% of the seeds had emerged. Flats were placed into one of two Conviron PGW36 (Conviron, Winnipeg, Canada) growth chambers, one with a temperature regime of 25/19°C and the other a 12/6°C day/night temperature regime. Each chamber was maintained at 14-h daylength and 512 ± 16 µmol m–2 s–1 light intensity. Plants were fertilized weekly with Miracle Gro fertilizer (Scotts Miracle-Gro Products, Inc., Port Washington, NY) at a rate of 1.875 g of fertilizer L–1 of water applied. Plants were checked daily and watered to prevent water deficit. At week 0, 12 flats (three from each temperature regime) were randomly selected and removed from the growth chambers. Plants were removed from the flat, their roots were washed with tap water, and the pseudostem was removed from the attached seed. The pseudostem and leaf tissue were frozen and freeze-dried using a Freezemobile 25SL Freeze drier (Virtis Inc., Gardiner, NY) and dry weights recorded. After 3 wk, three flats from each temperature regime were randomly selected and harvested as previously described, except a 2-mm cross section of the pseudostem base was analyzed for endophyte presence. In addition, three of the six remaining flats from the 25/19°C regime were randomly selected and placed into the 12/6°C temperature regime, and three of the six remaining flats from the 12/6°C regime were randomly selected and placed into the 25/19°C temperature regime. Plants were grown for an additional 3 wk, harvested, and analyzed for endophyte presence and freeze-dried as previously described.
Freeze-dried materials were analyzed for endophyte concentration using ELISA (Hiatt and Hill, 1997) and the tiller cross-sections analyzed for endophyte presence by immunoblot. Endophyte frequency was not determined on plants from week zero because plants were too small for immunoblot analysis. The experiment was replicated by randomly reassigning temperature regimes to the two growth chambers and conducting the experiment exactly as previously described. Data were analyzed using the PROC MIXED subroutine of the analysis of variance program of SAS. The experimental design was a randomized complete block with two replicates. Temperature regimes and harvest dates were considered fixed effects. Treatment means were separated using a Fisher's protected LSD at = 0.05.
Determining Cardinal Minimum Temperature for Endophyte and Tall Fescue Growth
Seeds of Jesup MaxQ were placed in water and refrigerated for 7 d to break dormancy. Seventy-two seeds were planted into each of 21 flats containing a commercial germinating mix and placed in a greenhouse. Germination date was recorded as Day 0 when 50% of the seeds had emerged. Six flats of 7-d-old seedlings were randomly assigned to each of three Conviron PGW36 growth chambers. The growth chambers had constant temperatures of 10, 15, or 20°C randomly assigned to them. Each maintained 14 h daylength and 516 ± 14 µmol m–2 s–1 light intensity. Plants were fertilized weekly with Miracle Gro fertilizer at a rate of 1.875 g L–1 of water applied. Plants were checked daily and watered to prevent water deficit. Each week for 6 wk, one flat of seedling plants was randomly selected from each growth chamber from which 50 plants were randomly selected and harvested. Harvested plants were removed from the flats, their roots washed with tap water, and the roots excised at the pseudostem base. A 2-mm cross section of the pseudostem base was made with a razor blade to determine endophyte presence, and the remaining excised plant freeze-dried. Plant dry weight was recorded. Freeze-dried materials were analyzed for endophyte concentration using ELISA (Hiatt and Hill, 1997) and tiller cross sections analyzed for endophyte presence by immunoblot. Endophyte frequency was not determined on plants from week 0 and 1 because plants were too small for immunoblot analysis.
The experiment was replicated by randomly reassigning temperature treatments to the three growth chambers and conducting the experiment exactly as previously described. Data were analyzed using the PROC ANOVA subroutine of analysis of variance of SAS. The experimental design was a randomized complete block with two replicates. Temperature treatments and harvest dates were considered fixed effects. Treatment means were separated using a Fisher's protected LSD at = 0.05.
The number of growth chambers available for determining minimum cardinal temperature for the tall fescue plant and endophyte was limited and, thus, confidence for a calculated cardinal minimum temperature for endophyhte was suspect and without published data from which comparisons could be made. Therefore, two mathematical models were used to estimate cardinal minimum temperature for endophyte growth. The first estimation was performed by regressing endophyte biomass data from weeks four, five, and six (dependent variable) with temperature (independent variable) using a quadratic formula and extrapolating the regression equation and solving for Y = 0. The second method used linear regression to fit the endophyte mass data (dependent variable) with temperature data (independent variable) using data from plants grown at 10 and 15°C and a second set of regression equations using data from plants grown at 15 and 20°C. The slopes (dependent variable) were fit to a linear regression equation with the average temperature (12.5 and 17.5°C; independent variable) and the linear equation solved for Y = 0. Solving for Y = 0 provided an estimate of when the slope was zero which, in turn, was an estimate of the minimum temperature for endophyte growth. The third method used to predict endophyte cardinal minimum temperature was an iterative least squares parameter search to find the best fitting exponential function for each week in the form:
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where Y = endophyte biomass and T = temperature. Endophyte mean cardinal minimum temperature and standard deviation were calculated for each method of regression analysis.
Plant dry weight (dependent variable) was regressed with temperature (independent variable) for samples harvested during weeks 4, 5, and 6 using linear and quadratic models in the PROC REG procedure of SAS. Cardinal minimum temperature for tall fescue growth was determined by extrapolating the best-fit regression equations (e.g., the highest order polynomial with a statistically significant coefficient) and solving for Y = 0.
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RESULTS
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Experiment 1. Seasonal Variation of Endophyte in Field-Grown Tall Fescue
Mean monthly temperatures showed typical annual trends with progressive increases in temperature from January to August and progressive decreases in temperature from September to December (Fig. 1
). There was a month effect, but no year or month x year effect for endophyte frequency for tall fescue in Georgia. Endophyte frequency from April through December was greater than for other months in Georgia (Table 1). A significant month by pseudostem location interaction for endophyte frequency occurred among the Georgia samples. Generally, endophyte frequency was similar at the base and 3 cm above the base in tillers sampled from April through November (Fig. 2
). However, the pseudostem base had significantly higher endophyte frequency in tissue sampled from December through March. Endophyte concentration was similar in both years, with peak pseudostem concentration from June through November (Table 2). Endophyte concentrations in tall fescue pseudostems were least in January. Endophyte frequency had a positive correlation with Georgia mean monthly temperatures (r = 0.44). However, none of the endophyte parameters (frequency or concentration) were significantly correlated with precipitation in Georgia (r = –0.01).
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Fig. 1. Weather data for Watkinsville, GA, and Salem, OR, for months when tillers were sampled from field-grown plants. Bar graphs and line graphs indicate precipitation and mean monthly temperature, respectively.
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Table 1. Mean monthly endophyte frequency in pseudostems of field-grown tall fescue in Georgia (2000 through 2002) and Oregon (1999 through 2001).
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Fig. 2. Mean endophyte frequency in pseudostem bases (bottom) and 3 cm above the pseudostem base (middle) of endophyte-infected tall fescue grown in Georgia fields during 2000 through 2002. Vertical bars on line graph indicate the value for Fisher's protected LSD at the 0.05 level of probability.
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Table 2. Mean monthly endophyte concentration in pseudostems of tall fescue grown in Georgia during 2000 through 2002.
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There was a month effect, but no year or month x year effect for endophyte frequency for tall fescue in Oregon. Endophyte frequency was similar when sampled from October through January, but least when sampled from February through April. Endophyte frequency had a positive correlation with Oregon mean monthly temperatures (r = 0.75). However, endophyte frequency was not correlated with Oregon precipitation (r = –0.18).
Experiment 2. Temperature Effects on Endophyte Growth
Growth Response of Endophyte and Tall Fescue under Different Temperature Regimes
Initially, all temperature treatments had similar low plant dry weight, but plant dry weight increased over time in all temperature treatments (Fig. 3
). At wk 3, plant dry weight was similar within treatments receiving either 25/19 or 12/6°C temperature regimes, but lower if grown at 12/6°C. Plants grown in the cool temperature regime for the duration of the experiment had the lowest final weight. Plants grown at 12/6°C and switched to 25/19°C at the end of 3 wk had greater final plant dry weights than those continuously grown at the cooler regime, but less than those continuously grown in the higher temperature regime. Final plant dry weight was less if plants grown in the 25/19°C regime were switched to the 12/6°C regime during the second 3-wk period.
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Fig. 3. Dry weight of tall fescue grown under four temperature regimes over a 6-wk period. One-half of plants were switched from one temperature regime to the other at Week 3. Vertical bars on line graph indicate the value for Fisher's protected LSD at the 0.05 level of probability.
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Initially, all temperature treatments had similar endophyte concentration and endophyte biomass. After 3 wk of growth, endophyte concentration was similar within treatments receiving either 25/19 or 12/6°C temperature, but endophyte concentration in plants receiving the 25/19°C regime had approximately 12 times the concentration of those receiving the 12/6°C regime (Fig. 4
). Endophyte concentration increased over the duration of the experiment when plants were grown in a continuous 25/19°C regime. However, endophyte concentration decreased if plants grown at 25/19°C were switched to the 12/6°C regime during the second 3-wk period. Plants continuously grown in the 12/6°C regime had similar endophyte concentration over the duration of the experiment. However, if they were switched to the 25/19°C regime at Week 3, endophyte concentration increased compared with those continuously grown at 12/6°C.
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Fig. 4. Endophyte concentration in pseudostems of tall fescue grown under four temperature regimes over a 6-wk period. One-half of plants were switched from one temperature regime to the other at Week 3. Vertical bars on line graph indicate the value for Fisher's protected LSD at the 0.05 level of probability.
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Endophyte biomass increased over the duration of the experiment when plants were grown at the 25/19°C regime (Fig. 5
), but final endophyte biomass was less if plants grown at 25/19°C were switched to the 12/6°C after 3 wk. Plants grown at 12/6°C regime had little or no increase in endophyte biomass during the 6-wk period. However, endophyte biomass increased when plants were switched from 12/6°C to the 25/19°C regime after 3 wk.
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Fig. 5. Endophyte biomass in tall fescue plants grown under four temperature regimes over a 6-wk period. One- half of plants were switched from one temperature regime to the other at Week 3. Vertical bars on line graph indicate the value for Fisher's protected LSD at the 0.05 level of probability.
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Endophyte frequencies for plants grown at all temperature regimes were similar, except when plants were continuously grown at 12/6°C for the entire 6-wk period (Table 3).
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Table 3. Effect of temperature and harvest date on endophyte frequency in pseudostems of tall fescue grown at four temperature regimes in growth chambers.
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Determining Cardinal Minimum Temperature for Endophyte and Tall Fescue Growth
Germinated plants had insufficient growth to test for endophyte presence during Weeks 0 and 1. There were no differences among temperatures or weeks, and there was no interaction between temperatures and weeks for endophyte frequency; however, there was a temperature by week interaction for plant dry weight, endophyte concentration, and endophyte biomass.
Although dry weights for plants grown at different temperatures were similar for Weeks 1 and 2, plant dry weight generally increased thereafter (Fig. 6
). Plants grown at 20°C grew faster than those grown at 15°C, which grew faster than those grown at 10°C. Endophyte biomass had a similar growth trend as plant dry weight when grown at 20 and 15°C, but plants grown at 10°C had little increase in endophyte biomass (Fig. 7
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Fig. 6. Dry weight of tall fescue plants grown at constant temperatures of 10, 15, or 20°C over 6 wk. Vertical bars on line graph indicate the value for Fisher's least significant difference at the 0.05 level of probability.
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Fig. 7. Endophyte biomass in tall fescue grown at constant temperatures of 10, 15, or 20°C over 6 wk. Vertical bars on line graph indicate the value for Fisher's protected LSD at the 0.05 level of probability.
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Plant dry weights (dependent variable) were regressed against temperatures (independent variable) for the week 4, 5, and 6 harvest dates. These data were best fit to a linear equation with r2 > 0.94 regardless of week when plants were harvested. The calculated X values for all three equations at Y = 0 had a mean of 5.2°C and confidence interval (p = 0.95) of ± 0.5°C. Extrapolations to zero plant growth suggest the cardinal minimum temperature for plant growth is approximately 5.0°C.
When endophyte biomass data (dependent variable) were regressed against temperatures (independent variable) using quadratic, linear, and the iterative least squares parameter search methods, all three methods of analysis indicated the cardinal minimum temperature for endophyte growth was higher (approximately 10°C) than that for plant growth (Table 4).
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Table 4. Predicted cardinal minimum temperatures for endophyte growth when calculated using three methods of regression analysis. Values represent the means of the calculated values when plants were grown in environmental chambers for 4, 5, and 6 wk. Values in the parentheses are the standard deviations of those means.
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DISCUSSION
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The impetus for this project was an observation that field-grown endophyte-infected plants had numerous tillers in which no endophyte was present. These plants were growing under dry and cool conditions in March 1998. A literature search found virtually no research linking environmental conditions with endophyte transmission. Thus, these experiments were conducted to perform initial investigations into environmental influences on endophyte grown in planta.
Di Menna and Waller (1986) noted seasonal variation in endophytes of perennial ryegrass grown under field conditions in New Zealand. They found fewer mycelia in pseudostem tissue during August, the equivalent of February in the Northern Hemisphere. Their data suggested that seasonal variability in perennial ryegrass was similar to the data for field-grown tall fescue in Georgia and Oregon in this study. Although not tested, they attributed the seasonal variation to temperature and drought stress. Bacon and Siegel (1988) noted a decrease of endophyte in seed and vegetative tissue of tall fescue after the plants had experienced hot and dry summers and cold winters.
Responses of tall fescue grown under constant temperature regimes of 10, 15, or 20°C, or when transferring plants from warm to cool or cool to warm conditions, were similar to that found by others (Robson, 1974; Thomas and Stoddart, 1995). Plants grown at high temperatures had greater growth than those grown at cooler temperatures. Plants switched from warm to cool conditions reduced growth rate, while those switched from cool to warm had increased growth rates (Fig. 3 and 6). Although extrapolation of regression was used to estimate the cardinal minimum temperature for plant growth weight, our estimated cardinal minimum temperatures of 5.2 ± 0.5°C for plant growth was similar to that determined by Thomas and Stoddart (1995). The similarity of our test results with that of others provides a measure of confidence that the test conditions for experiments investigating temperature effects on plants reported herein are valid.
The calculated cardinal minimum temperature for endophyte growth was approximately 10°C, or 5°C higher than that for plant growth. Thus, it is not surprising to find lower endophyte frequencies in field-grown tall fescue during the winter and spring months (Table 1) when mean monthly temperatures were often below the cardinal minimum temperature for endophyte growth, yet above the minimum temperature for plant growth. It is important to note, however, that while endophyte frequency and concentration were lowest in months when temperatures were lowest, it is possible that the endophyte response is related to vernalization and physiological or morphological changes occurring in the plants. The endophyte resides within meristematic tissue during vegetative growth (Sampson, 1933, 1937; Bacon and Siegel, 1988) and in flower primordia before inflorescence development (Siegel et al., 1984). Hinton and Bacon (1985) suggest that infected flower primordia may outgrow the endophyte during stem elongation. Thus, it is vital for endophytes to invade seed and culm primordia to avoid having to maintain rapid growth rates during elongation of the culm. Endophytes have been observed in differentiating flower primordial tissue of perennial ryegrass before stem elongation (Philipson and Christey, 1986). Thus, it is likely the endophyte prioritizes invasion of the developing floret over other tissues, perhaps when vernalization conditions have been met. Because the endophyte in planta is nonseptate (Hinton and Bacon, 1985), it is possible the endophyte can mobilize vital components (proteins, carbohydrates, etc.) from mycelium in above ground tissue to the plant meristem to provide necessary nutrients where they are needed for invasion of the developing panicle primodia during plant vernalization.
From a practical standpoint, this research demonstrates that tall fescue should not be sampled for endophyte detection from January through April. This is an important finding since many producers are likely to sample pastures for endophyte frequency to guide their management decisions concerning pasture renovation and use. Pastures should be sampled from May through December in the northern hemisphere to obtain valid endophyte frequency data from which to base these management decisions.
Received for publication April 7, 2005.
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ABSTRACT
INTRODUCTION
